Extreme tolerance for nocturnal emergence at low body temperatures in a high-latitude lizard: implications for future climate warming

High-latitude lizards are capable of activity at low winter temperatures and are active on warm nights (including in winter) with prior warmer temperatures during the day, with active field body temperature as low as 1.4#x00B0;C and air temperature less than 1#x00B0;C.


Introduction
Activity in ectotherms is primarily dependent on their immediate thermal environment (Sound and Veith, 2000;Angilletta, 2009). Ectotherms make the best use of their immediate environment when weather variables such as air temperature, solar radiation, cloud cover, wind and photoperiod are favourable for activity (Gordon et al., 2010;Vermunt et al., 2014). Extremes of these variables result in a significant decline in fitness , and a persistent change in weather variables can be lethal, for example leading to cold death (Stroud et al., 2020) or local extinction (Huey and Tewksbury, 2009;Sinervo et al., 2010). In extreme cold at near-freezing temperatures, metabolic rate of reptiles falls to low levels, contraction of isolated muscles declines and locomotory ability eventually ceases (Paladino, 1985;Storey, 2006;James, 2013).
Although temperature plays a fundamental role in determining when squamates are active, including when thermoregulating, foraging or even mating (Adolph and Porter, 1993;Autumn et al., 1994;Logan et al., 2015;Gunderson and Leal, 2016), other factors, including wind, solar radiation and water availability, are also influential. For example, wind can counter the effect of warm temperatures on lizards through convective cooling of the skin surfaces; it can force squamates to remain in a retreat by decreasing air and substrate temperature and also by affecting water relations (Kearney and Porter, 2009;Ortega et al., 2017). Thus, wind can reduce activity time, thermoregulatory efficiency and thermal quality (Logan et al., 2015;Ortega et al., 2017). Water availability is also a strong predictor of activity in squamates and high rates of evaporative water loss can restrict activity, which helps avoid further water loss. Lizards' activity increased after a heavy rainfall event (Kearney et al., 2018) and low water availability such as a dry spell can result in reduced activity with animals remaining in retreats (Crowley, 1987;Lorenzon et al., 1999;Kearney et al., 2018). Vapour pressure deficit (VPD) facilitates water loss through the integument due to its drying power, forcing an animal to remain in its retreat (Kearney et al., 2018). However, the effect of VPD may be less noticeable at night and not predict activity patterns of nocturnal squamates due to the lower temperatures.
Furthermore, in some species, activity is not only dependent on weather variables, but also on ecological needs and functions (Brown and Shine, 2002) and on life history traits such as differences between juveniles and adults (Adolph and Porter, 1993). Behavioural plasticity can also help shape lizard activity, even when weather conditions are favourable (López-Alcaide et al., 2017). Regardless of how they are influenced, activity periods determine how the ecological niches of lizards are shaped, including how lizards interact with competitors for mates and food resources and, potentially, their exposure to predators (Anholt et al., 2000;López-Alcaide et al., 2017). However, for higher latitude cool-climate lizards, how weather conditions shape activity, the influence of life history group (which can include body size differences) on these patterns and the extent to which cold winter weather forces these species to remain in retreats remain unclear.
Nocturnality poses particular constraints on activity of some high-latitude ectotherms. In general, nocturnality signals an ability to be active at relatively low nighttime environmental temperatures (Hare et al., 2005) and at low body temperature (Autumn et al., 1994); it brings advantages in reducing dietary competition with sympatric, diurnal organisms (Vitt et al., 2003) and in reducing exposure to primarily diurnal, visually oriented predators (Gaston, 2019), while still allowing high body temperature (T b ) to be achieved during the day (Huey et al., 1989). Despite experiencing relatively low and variable temperatures for activity at night, when T b typically falls below preferred body temperature (Huey et al., 1989;Autumn et al., 1997), nocturnal lizards can still be capable of high locomotory function (Autumn et al., 1997). High levels of nocturnal activity are apparent in some ectotherms where air temperatures are high (Weatherhead et al., 2012;Sperry et al., 2013), but even at higher latitudes with low (∼8 • C) air temperature at dusk, field activity in cold-adapted species can be high at night . Nonetheless, a cessation of activity throughout winter at high latitudes is often observed with high-latitude lizards remaining in retreats during normal activity time.
Thus, increased nighttime temperature could be beneficial to cool-temperate lizards by creating a thermal environment that enhances activity. Increased nighttime temperature is particularly driven by increasing cloudiness during the day, which helps retain heat on the surface (Cox et al., 2020). As climate change raises temperatures (including nocturnal temperatures) and affects other weather conditions around the globe (IPCC, 2021), it becomes important to understand the ways that current and future conditions might affect activity of ectotherms, including nocturnal, high-latitude species Johansson et al., 2020).
Here, we investigated the nocturnal activity pattern of a cold-adapted, viviparous gecko known by the tag name Woodworthia 'Otago/Southland' (Nielsen et al., 2011;Hitchmough et al., 2021), at a subalpine site (Macraes) in southern Aotearoa New Zealand, to understand how current weather conditions influence nocturnal emergence. This rock-dwelling taxon is recognized as a nocturnal forager (Whitaker, 1984;Spencer and Grimmond, 1994), though it has an unusual activity pattern at our study site in being active outside the retreat not only at nighttime but also when basking cryptically during the day at the retreat entrance (Gibson et al., 2015); such basking, seen almost entirely in pregnant females (Chukwuka, 2020), helps elevate T b both in the field and the laboratory and thereby hastens embryonic development (Cree and Hare, 2016a). Ambient air temperature at Macraes is frequently below the geckos' preferred body temperature (Rock et al., 2000) and also below retreat-site temperature (Chukwuka et al., 2021) (Chukwuka et al., 2019), the way that current weather conditions shape nighttime emergence activity and field body temperature, including whether these patterns differ intraspecifically, remains unclear.
We assessed the seasonal variation in operative environmental temperature (T e ) available to geckos when they emerged in the open at night using dataloggers inserted into lizard models. Concurrently, we assessed nighttime emergence activity using time-lapse trail cameras (thus eliminating any effect of observer presence). We explored whether weather conditions influence field T e and nocturnal emergence and whether the effects vary with season, time after dusk, retreat type and life history group (adult versus juvenile, male versus female). We predicted that activity in these geckos would be high in spring and summer when the air temperature is high compared to winter and that geckos would be inactive in winter due to low temperatures. We also predicted that geckos' emergence from thin rock slabs would be less than from thick rock slabs and deep crevices. Thin rock slabs cool rapidly at dusk and geckos may select retreats with more stable temperatures at night (Chukwuka et al., 2021). Nighttime emergence was also predicted to be higher on nights with prior warmer daytime temperatures than following cold days. We also quantified the field body temperature (T b ) of emerged geckos of different life history groups at night, using a thermal infrared camera, to understand how weather conditions and nighttime rock surface temperature affect field T b . For emerged geckos, we predicted that night field T b would be higher than the T a and closer to rock surface temperature, noting that rock surfaces can remain warmer than air temperature following warm days and this warmth would be beneficial to gecko activity. In addition, we predicted that larger geckos (adults) and pregnant female geckos would have higher T b that is more independent of T a (more similar to retreat-site temperature) in the first few hours after dusk than small geckos (juveniles) and other life history groups, respectively, and that these trends would be seasonally dependent. We expected these differences in T b given the effects of body size on rate of heat loss and given the higher thermal preference of geckos during pregnancy, which hastens embryonic development (Rock et al., 2000;Cree and Hare, 2016b). Our study provides a detailed insight into activity patterns under the current climate and insight into future possible impacts of climate change.

Study site
Our study was conducted near Macraes township (−45 • S, 550-710 m asl), eastern Otago, Aotearoa New Zealand, between May 2017 and April 2019. Field sampling was conducted in two adjacent locations: The Department of Conservation's Redbank Reserve for surveys of nighttime field body temperature and nearby private land for filming, both within 4 km of one another. The rock tors in these field sites have loose slabs and horizontal cracks (deep crevices) inhabited by geckos (Rock et al., 2002), and surrounding the tors at the base are tussock grasses and some fruiting shrubs, including Chionochloa rubra, C. rigida and Festuca novaezelandiae.

Measurement of nighttime operative environmental temperature
We deployed six hollow copper models calibrated against gecko body temperatures  to measure operative environmental temperature (T e ) available to emerged geckos at night (Bakken, 1992). Thermocron iButtons (DS1921G-F5#, resolution ±0.5 • C from −30 • C to +70 • C, recording hourly) were inserted into each copper model, and the model was sealed with ultraviolet-resistant tape (Rock et al., 2000;Dzialowski, 2005). Each copper model was glued to a terracotta tile and positioned on a rock tor close to a retreat-site entrance. T e was measured concurrent with the activity filming and is presented for the first 5 hours after dusk; this was the period when nocturnal activity was at its peak (Christian Chukwuka, pers. obs.).

Patterns of nocturnal emergence of geckos using trail cameras
We conducted field surveys for 28 days in each season using nine trail cameras (Reconyx™ wildlife cameras) in three types of retreats: thin loose slabs (thickness: ≤4.5 cm), thick loose slabs (thickness: ≥4.6 cm) and horizontal crevices of >0.4 m deep within rock outcrops (Chukwuka et al., 2021). At the start of the first season of filming in spring, turnable rock slabs (thick and thin loose slabs) were turned to confirm that at least one or more geckos from each life history group (adult male and female, snout-vent length (SVL) ≥ 68 mm; and juvenile, SVL < 68 mm) were present (Rock et al., 2000). Geckos inside deep crevices were not able to be captured or marked. The geckos captured under the turnable rock slabs were marked with a non-toxic silver pen in the spring season only, on both flanks, for easy identification in the photo frame. The geckos were returned to the capture site immediately after handling.
The cameras were mounted on metal stakes with a ballhead camera mount and positioned level with the retreat site at a 1-m distance from the rock tor (one camera per crevice or slab); they were then set using a time-lapse function to capture photos of the retreats and their surroundings (Hobbs and Brehme, 2017), using infrared night vision. We used a time-lapse function rather than motion sensors due to the geckos' small body size and insufficient temperature difference from background temperature (Welbourne et al., 2017). The images were processed using online free software, Timelapse2, which collates data directly to an Excel sheet (Greenberg, 2017). We played a series of photo frames to detect geckos by looking for eye shine and movement of geckos among frames. The camera footage from dusk until 5 h after dusk was examined to assess the geckos' nocturnal activity; nocturnal emergence was taken as the appearance of half or more of the gecko's body outside the retreat. The number of geckos seen emerged in each frame and emergence duration, inferred from the presence of a gecko in the same position on images at 1-min intervals, were quantified. Due to the inability to differentiate between adult sexes and reproductive conditions of the geckos from the monochrome photos, we categorized the life history group only as an adult or juvenile for this aspect of the study.
All the footage was examined twice by one person for the presence or absence of geckos in each image. We assumed that likelihood of detecting geckos was constant for all the photo frames. There was no data loss or camera malfunction for the nine cameras installed, except when one camera was attacked by a non-native brushtail possum, Trichosurus vulpecula, during the spring season. As this disturbance changed the field of view for 10 recording days from the targeted rock slab, these recordings were excluded from the analysis.

Field body temperature and rock-tor surface temperature at night
At an adjacent site, we sampled emerged geckos at night to measure field body temperatures in each season. Using spotlights for the 5 h after dusk, we detected geckos from a distance by eye-shine or from their bodies at closer approach (Lettink and Monks, 2016). We measured skin surface temperature (dorsal abdomen) using a thermal infrared camera (IRC, Flir i60) or with a mini-infrared thermometer without touching or disturbing the gecko (Chukwuka et al., 2019). The two devices were used interchangeably because the IRC battery depleted before the night survey started on some days. The data measured with the two devices were standardized using a calibration equation in Chukwuka et al. (2019). We captured the geckos to measure their SVL to differentiate adults and juveniles and also determined the females' reproductive status (Rock et al., 2000;Cree and Hare, 2016b). We distinguished sex of adults by the presence of a hemipenial sac at the base of the tail as well as pre-anal and femoral pores anterior to the cloacal opening in males. We distinguished female reproductive condition (pregnant vs non-pregnant) by palpation. We released the geckos at the same site within 1 min of capture.
In addition, we also measured the rock-tor surface temperatures surrounding where the geckos were captured to infer substrate temperature at night. A circular region of interest (ROI) was drawn around the geckos and the maximum temperature within the ROI was taken as the substrate temperature where geckos were captured.

Field retreat temperatures
Daytime field retreat temperatures (T retreat ) were measured using Thermocron iButtons to test whether it predicts emergence at night. Six Thermocron iButtons were installed in each of three different retreat types, i.e. thick and thin rock slabs and deep crevices Chukwuka et al., 2021), using duct tape. For the deep crevices, iButtons were inserted ∼0.4 m depth with insulated metal wires. We set the iButtons to measure the temperature every hour and analysed data from the first five hours after dusk to be consistent with filming.

Climate data
We obtained weather conditions (air temperature, rainfall, relative humidity and wind speed) recorded every 60 min during the study period at the weather station (Fire and Emergency New Zealand, FENZ) located ∼ 2 km from the study sites from National Institute of Water and Atmospheric Research. Solar radiation data measured hourly using a pyranometer installed beside the FENZ weather station were also obtained (Evie Virens, University of Otago, pers. comm.).

Data analysis
All data were analysed in R package (R version 3.5.3), and plots were generated with the 'ggplot2' package in using Rstudio interface (R Core Team, 2008). Data were presented as mean ± standard error with the confidence limit set at 95%. We tested for homogeneity of the dataset using the plot of residuals in 'autoplot' function in R. All skewed data were log-transformed before the final analysis. For significant results, effect sizes (Hedges g) were calculated to compare mean differences and interpreted as very small (0.01-0.19), small (0.20-0.49), medium (0.50-0.79), large (0.80-1.20) and very large (>1.20) (Sawilowsky, 2009).

Field operative temperature
We analysed the hourly mean field T e using multiple linear regression to determine the influence of current weather conditions (Shine and Kearney, 2001). Mean differences in T e across seasons and times of day were compared using a two-way ANOVA. We calculated the drying power of the air, i.e. VPD, using temperature and relative humidity (Jucker et al., 2018). We presented T e relative to a measure of preferred body temperature calculated for the same population of geckos from the raw data of a published study (Rock et al., 2000), to infer if the activity temperature matches the gecko's preferred body temperature. We calculated the 50th percentile of the preferred body temperature selected by the geckos at 21:30 h in spring and summer for adult geckos.

Nighttime emergence in relation to season, time of night and weather conditions
To understand the influence of weather conditions (air temperature, wind speed, VPD and rainfall) on counts of gecko sightings per hour within 5 h after dusk, we modelled camera data with a generalized linear mixed model using template model builder as implemented in the R package glmmTMB (version 1.1.5) using the functions, glmmTMB and a nbi-  (Booth et al., 2003;Brooks et al., 2017). The 'glmmTMB' package estimates zero inflation in a dataset and models random effects following repeated sampling using Laplace approximation (Brooks et al., 2019). The excess zeros in the dataset were regarded as a true zero because the frequency of gecko activity depends on real ecological effects such as suitable weather variables for activity and the presence/absence of predators around the retreats (Welsh et al., 1996;Martin et al., 2005). For this model, season and retreat type were included as fixed factors. We checked for multicollinearity using variance inflation factor score, and T e was removed from the final model due to collinearity with T a . We retained T a rather than T e in the model as it is from the same weather station/location and points in time as the other weather variables used in the analysis. Also, the effects of the season, retreat type and life history stage (adult or juvenile) on the duration of nocturnal emergence were modelled using a separate glmmTMB model. For all these models, camera identity was included as a random factor. We included interaction terms for variables that have biological significance.
Also, we tested how warmer daytime temperature (daytime T a ) influenced the nocturnal emergence of the geckos using a generalized linear model with counts of gecko emergence at night as the dependent variable and mean daytime air temperature as a predictor variable. We included seasons in the model as a fixed co-factor. We also calculated the difference between the daytime mean air temperature and both nighttime T retreat and T e to test whether these variables affected the number of lizards that emerged from the retreat at night.

Active field body temperature
To understand how season and life history group influenced nighttime field body temperature, we performed a two-way ANOVA using mean field T b as a response variable. For the body temperature analysis only, the time when the geckos were captured was included as a covariate. We also performed a linear regression to establish relationships between the gecko's field body temperature and nighttime air temperature and between T b and substrate temperature where the geckos were captured to identify the best predictor of field T b . Also, the influence of weather conditions on nighttime field body temperature was modelled simultaneously using multiple linear regression, with the season and hours after dusk as fixed factors.

Field operative temperatures
The nighttime operative environmental temperature (T e ) during the filming periods reached highest values in summer (mean maximum, 21.7 • C) and lowest in winter (mean minimum −1.92 • C) and differed significantly in autumn and winter compared to spring and summer (χ 2 = 557.06, df = 3, Figure 1: Hourly mean operative temperatures (T e ) on the exposed rock surface during 28 days of each season at Macraes, Otago, New Zealand. Mean T e differed significantly across the seasons and with time after dusk (P < 0.001). There was also a significant interaction (P < 0.001), with the effect of time after dusk being greatest in spring and summer. Data were collated only for the first 5 hours after dusk when the activity of geckos was high in the field. N = 6 copper models. Standard errors are small and within the size of the plot shapes. The dotted line represents the 50th percentile of preferred body temperature selected by the same population of geckos at 21:30 hr in spring and summer (Rock et al., 2000). P < 0.001; Figure 1). The mean maxima of the T e were always below the geckos' preferred body temperature (25 • C) from a published study (Rock et al., 2000) in all the seasons. T e showed a decline from the first hour after dusk until the fifth hour (χ 2 = 18.02, df = 1, P < 0.001), the decline being greater in spring and summer than in autumn and winter (season * time after dusk: χ 2 = 5.83, df = 12, P < 0.001).
All the weather conditions influenced the field T e (P < 0.001, Table 1), with a positive relationship between T e and air temperature (r = 0.69) and a negative relationship between T e and wind speed (r = −0.23, Supplementary information Figure S1). The relationship between T a and T e was affected significantly by wind speed, VPD and amount of rainfall (P < 0.001, Table 1).  after dusk. Most geckos sighted at night were adults (88%) rather than juveniles (12%). The number of gecko sightings in every 60 images (1 h) of footage varied significantly with season (χ 2 = 22.27, df = 3, P = < 0.001) and with time after dusk (χ 2 = 172.80, df = 4, P < 0.001; Figure 2, Table 2). Emergence was relatively high in spring and summer (means up to 33 sightings per hour in spring) but reduced in autumn and winter (means up to 17 sightings per hour; Figure 2). No significant effect of retreat type (thick rock slab, thin rock slab or deep crevice) on mean number of geckos sighted was observed (χ 2 = 1.36, df = 2, P = 0.51). However, there were more sightings of geckos that emerged from deep crevices in summer and winter than for other retreat types (interaction of season with retreat type: χ 2 = 33.19, df = 6, P < 0.001). A larger number of geckos were sighted in the first 2 hours after dusk in summer than at other times (interaction of season with time after dusk: χ 2 = 706.27, df = 12, P < 0.001).

Nighttime emergence in relation to season, time of night and weather conditions
Nocturnal emergence increased with increasing air temperature at the time of emergence (χ 2 = 56.71, df = 1, P < 0.001) and with decreasing wind speed (between 0 and 5 m/s; χ 2 = 31.41, df = 1, P < 0.001; Table 2, Figure S2). VPD and rainfall did not predict gecko emergence at night (P > 0.05 for both; Table 2, Figure S2). The effect of air temperature on nocturnal emergence also depended on the combined influence of air temperature and wind speed (air temperature: wind speed, χ 2 = 27.28, df = 1, P < 0.01).

Nighttime field active body temperature and rock surface temperature
The highest nighttime field T b when emerged was recorded in spring for a pregnant female (22.6 • C) and the lowest in winter for a non-pregnant female (1.4 • C; Figure 4A). Most of the captured geckos were found motionless either on vegetation or a rock tor. Juveniles were sometimes present at high numbers (up to 16 juveniles) within the shelter of a golden spaniard plant (a type of spear grass, Aciphylla aurea). Mean field T b differed significantly across the seasons (χ 2 = 446.20, df = 3, P < 0.001), being lower in summer compared to spring, and with time after dusk (χ 2 = 5.76, df = 1, P = 0.01; Figure 5  Woodworthia 'Otago/Southland' geckos during nighttime emergence at Macraes, Otago, New Zealand. In winter, emerged geckos were sighted only from deep crevices. In summer, no emerged gecko was sighted from under thin rock slabs. The nocturnal emergence duration differed significantly across seasons (P = 0.001) but not among retreat types (P = 0.62). However, the interaction of season and retreat type was significant (P = 0.02). The emergence duration was inferred from the presence of a gecko in the same position on images per trail camera taken at 1-min intervals.
Nighttime field T b (mean: 7.41 ± 0.10 • C) was significantly lower than rock surface temperature measured from the same spot where geckos were captured at night (mean: 8.58 ± 0.02 • C; χ 2 = 637.45, df = 1, P < 0.001; Figure 4B), with a strong positive relationship (R 2 = 0.84, P < 0.001; Figure 6A). In addition, there was a positive effect of air temperature (mean air temperature: 6.56 ± 0.001 • C) and VPD (mean VPD: 0.13 ± 0.84 kPa) on the geckos' nighttime field T b (air temperature: F 1,286 = 613.84, P < 0.001; VPD: F 1,286 = 61.27, P < 0.001; Figure 6B,C), but no effect of wind speed (mean: 3.8 ± 0.08 m/s; F 1,284 = 0.12, P = 0.72). The overall effect of thermal variables on field T b is that the mean nighttime field T b is intermediate between the (warmer) rock surface and the (cooler) night air temperature. The effect of air temperature came close to being influenced by VPD (air temperature: VPD: F 1,284 = 3.35, P = 0.06; but not wind speed (air temperature: wind speed: F 1,284 = 0.30, P = 0.58). The effect of wind speed on nighttime field body temperature was influenced by the drying power of the air (wind speed: VPD, F 1,284 = 7.28, P = 0.007).

Discussion
Weather conditions at the time of sampling influenced the nighttime emergence of Otago/Southland geckos, with high emergence activity on warm nights. Operative environmental temperature (T e ) and emergence activity were high when air temperature was high and wind speed low. The number of emerged geckos sighted at night and the duration of emergence were highest in spring and summer (with T b up to 22.63 • C in spring) and continued (at low levels) during autumn and winter despite the cold climate. We also found that Otago/Southland geckos are active at night with field body temperature (T b ) as low as 1.4 • C when the air temperature was less than 1 • C in winter. At night, the maximum T e was below the gecko's preferred body temperature in all seasons (Rock et al., 2000).
Nocturnal activity in our study species is interpreted as a function of temperature, and to an extent, time after dusk. Although activity of lizards, in general, is associated with temperature (Huey, 1982), activity at such a low air temperature (<2 • C) is peculiar for mid-alpine Otago/Southland geckos (herein) and probably also for another New Zealand species, the orange-spotted gecko The lowest field T b observed (EI1: mean 1.4 • C for a nonpregnant female gecko found on vegetation). (B) A male gecko captured at the base of a rock tor that had a residual surface temperature (EI2: 6.3 • C; yellow triangle by the tail of the gecko denotes the warmest spot on the rock tor) higher than the gecko's body temperature (EI1: mean 3.8 • C). The circles (big, EI2 and small, EI1) represent the ROIs, the red and yellow triangles are the hottest, while blue and green triangles are the coldest spots within the ROI, respectively. The small circular ROI on the geckos'dorsum corresponded to the circumference of the sensor of a mini-infrared thermometer (Chukwuka et al., 2019).
(Mokopirirakau 'Roys Peak'), which was found active in the alpine zone, with lizard model temperatures averaging as low as −0.8 • C (Bertoia et al., 2021). In an Australian nocturnal gecko, Gehyra variegata, activity was high on warm nights (air temperature above 20 • C) and dropped sharply on cold nights with air temperature below 18 • C (Bustard, 1967). Activity at low nighttime temperatures may be costly for the lizards because low locomotory speed at a lower temperature would increase the risk of predation by endotherms Figure 5: Mean ± SE nighttime field body temperature of emerged geckos (Woodworthia 'Otago/Southland') measured within five hours after dusk at Macraes, Otago, New Zealand. The skin surface temperature of the geckos varied with the season (P = 0.0001) but did not differ significantly among life history groups (P = 0.12). The higher field body temperatures in spring compared to summer are explained by warmer air temperature on the sampling nights. Sample sizes for male, non-pregnant female, pregnant female and juveniles were as follows: Spring: 35, 15, 14 and 12, respectively;Summer: 37, 26, 21 and 27, respectively;Autumn: 23, 21, 6 and 21, respectively;and Winter: 12, 12, 1 and 14, respectively. (Cooper, 2000) and reduce the likelihood of prey capture (Hare et al., 2007;Gaby et al., 2011). To counter locomotory performance at low temperatures, nocturnal lizards may also have evolved a low minimal cost of locomotion by reducing muscle force and mechanical work (Farley and Emshwiller, 1996;Hare et al., 2007), and enhanced mitochondrial functions (Autumn et al., 1999). However, whether increased nighttime activity on warm nights in this study poses a predation risk to this species and other nocturnal lizards at high latitudes remains unclear. At high latitudes, it is likely that lizards are at less risk of predation by introduced mammalian predators (currently their main predators) at warmer night-time temperatures than at cooler temperatures when locomotion may be impaired. So, the consequences of increased nocturnal activity under climate change will probably depend both on how climate change affects mammal populations (e.g., allowing some species to become residents, and others to be in greater abundance, at higher elevations; O'Donnell et al., 2017) and on lizard biology (e.g., greater nighttime emergence (this study) and potentially also increased reproduction; Cree and Hare, 2016a).
High wind speeds reduced the nighttime emergence of Otago/Southland geckos; most sightings of emerged geckos occurred at low wind speeds. In studies on other lizards, wind facilitated the cooling of field T b through convection and may lead to a drop in body temperature when out of the retreat (Maia-Carneiro et al., 2012;Gontijo et al., 2018). In contrast, activity at high wind speed has been inferred for the diurnal lizard, Anolis lemurinus (Logan et al., 2015) but wind significantly reduced thermoregulatory set-point temperatures of a New Zealand diurnal skink in a controlled experiment (Virens and Cree, 2022) Relationships with the rock substrate temperature on rock tors where the geckos were captured at night. Rock substrate temperature was measured with a thermal infrared camera. Substrate temperature was statistically warmer than the gecko body temperatures (P < 0.001). (B) Field T b increased with increasing air temperature and was statistically warmer than the air temperature. (C) Field T b decreased as air become drier (increased VPD). The air temperature was measured concurrently with the field T b , with a Themocron iButton hung at 1 m above the ground. VPD was calculated from the air temperature above, and relative humidity data measured every hour at a nearby weather station at Macraes corresponding to the time when the field sampling was done (obtained from Fire and Emergency Services New Zealand). The grey-shaded area is the 95% confidence interval of the regression line. The broken red lines represent the isothermal line.
the activity of Woodworthia maculata (then described as Hoplodactylus maculatus) on Takapourewa/Stephens Island in New Zealand observed relatively low activity on nights with high wind speed (Walls, 1983). Due to moderate elevation (∼600 m) where our study population thrives, galeforce winds can interrupt lizard activity at night even if other weather factors such as temperature are favourable. As a consequence of wind, more body water may be lost due to evaporation from the integument (Waldschmidt and Porter, 1987), and communication between individuals will be impaired (Peters et al., 2007). High windspeed counters the thermoregulatory processes, decreases thermal accuracy and increases desiccation rates (Ortega et al., 2017).
Otago/Southland geckos were found active over a broad range of temperatures with lowest T b of 1.4 • C, which to our knowledge is the lowest field T b ever measured for an active lizard in New Zealand (Hare and Cree, 2016) or elsewhere in the world (Meiri et al., 2013). These geckos were either on vegetation or motionless on rock tors with rock surface temperature that was typically higher than the air temperature at low nighttime air temperatures. In our study, field T b is in general intermediate between T a and rock temperature, hinting that the geckos may have the opportunity to thermoregulate to a small extent (Nordberg and Schwarzkopf, 2019), by where they position themselves at night (because the tors store heat and there is thermal heterogeneity among the available microhabitats). The low night field T b in this study indicated that Otago/Southland geckos are capable of being active at an air temperature of less than 2 • C, well below their physiological optimum (Gaby et al., 2011). Most of the geckos captured at night were sluggish and were unable to move rapidly even after taking the body temperature measurement, suggesting that Otago/Southland geckos are 'sit-and-wait' ambush feeders, passively waiting for prey and capturing them without chase or pursuit (Spencer and Grimmond, 1994) as a result of low locomotory performance at low ambient temperature (Hare et al., 2007). In winter, a season when these geckos had been thought to be inactive/torpid (Hare and Cree, 2016), field sampling on 12 rock tors (nighttime air temperature: ∼4 • C) yielded up to 26 adult geckos active, and more than 18 juveniles were found on a golden spaniard (A. aurea). These juveniles may have been deriving a thermal benefit from the shelter provided by the speargrass, as well as foraging while avoiding predation.
Activity at such a low T b in the field was unexpected, although laboratory studies show that Otago/Southland geckos are capable of righting themselves at least as low as a T b of 0.8 • C when the air temperature was −0.5 • C (Besson and Cree, 2010). They have also been seen active at a room temperature of 5 • C in the laboratory (Vermunt et al., 2014). Activity at low nighttime body temperature in our field study may have been enhanced by high daytime temperature prior to the sampled nights (Walls, 1983), but clearly, the geckos are capable of functioning at low air and body temperatures. At low T b , movement and escape from predators are impaired (Bennett, 1980) due to reduced sprint speed (Gaby et al., 2011) crevices with more stable temperature conditions (Chukwuka, 2020), or they can tolerate low body temperatures (Bertoia et al., 2021) with a low cost of locomotion (Hare et al., 2007) and high aerobic capacity (Hare et al., 2010), though probably not allowing their body water to freeze (Claussen et al., 1990;Costanzo et al., 1995). The survival mechanisms at low ambient temperature, including whether Otago/Southland geckos are freeze-tolerant, remain unknown. We suggest further research to understand the physiological mechanisms at low temperatures in Woodworthia geckos and other New Zealand lizards living in similar cold microhabitats.
High-latitude lizards live in a heterogeneous thermal environment in which microclimate temperatures are frequently lower than the voluntary thermal maximum (Chukwuka et al., 2021). Thus, cool-climate lizards may be at less immediate risk than their tropical counterparts from overheating due to global climate change Clarke and Zani, 2012;Huey et al., 2012), although some microhabitats even within retreats have the potential to exceed VT max on hot summer days . Warmer conditions will enhance activity for high-latitude lizards when T e frequently remains below the optimum temperature (T o ), while the animal frequently explores the heterogenous microhabitat (Huey et al., 2012). In terms of activity, high-latitude lizards may initially benefit from future climate heating until fieldactive T b exceeds the optimum temperature (Huey et al., 2012). Currently, high-latitude lizards possess higher thermal safety margins, with lower active body temperature, critical thermal minimum and selected temperatures, and broader optimal temperature ranges (Besson and Cree, 2010;Gaby et al., 2011;Hare and Cree, 2016) compared to lower-latitude species (Huey, 1982;Clusella-Trullas et al., 2011;Sunday et al., 2014). Thus, mean activity levels for cool-temperate reptiles and amphibians will initially increase as climates warm (Buckley et al., 2012;Huang et al., 2013;Gade et al., 2020).
In New Zealand, future climate projections under representative concentration pathway 4.5 (a relatively optimistic scenario for greenhouse gas emissions) suggest that the region within which our Macraes field site falls will experience warmer temperatures with more extremely hot days (days with air temperature > 30 • C) in 2040 and 2090, reduced rainfall in summer and increased rainfall in winter and spring, decreased wind conditions by an average of −2.5% in 2040 and −1.5% in 2090 and a reduced number of frosty days (Macara et al., 2019). Winter temperatures are predicted to warm more rapidly than summer temperatures in the same year (Macara et al., 2019). Warmer night temperature, together with seasonal changes in rainfall pattern and reduced wind speed (with reduced cooling of the rock substrate), have the potential to increase the nocturnal activity of Otago/-Southland geckos. The increase in nighttime air temperature is predicted to persist over the winter season resulting in a probable increase in mid-winter nocturnal activity (herein), allowing geckos to forage and find mates more effectively. Warmer temperatures may also present growth and reproductive benefits (Kubisch et al., 2012;Cree and Hare, 2016a). However, the long-term consequences of increased climate heating (including the potential for harmful extremes of temperature) on activity timing, increase in winter rainfall and other important aspects of natural history including maternal gestation length and offspring phenotypic traits, remain unclear. Recent finding suggested that lizards at higher elevation will experience greater impact of climate change due to decrease in habitat availability especially for our study species (Jarvie et al., 2022); but consequences of increased warming may not be enormous when microclimate properties and lizards' biology are considered (Chukwuka et al., 2021). In addition, the potential for increased vulnerability to predation while emerging (Wilson and Cooke, 2004;Sperry et al., 2010), including from introduced mammals, which themselves will be impacted by climate change, will be important to address.

Funding
The study was supported by PhD grant (2016)

Data Availability Statement
The data used in this article is available on request to the corresponding author.